the functional design of the insect excretory system - The Journal of ...

4 S. H. P. MADDRELL
passively cross the walls of this insects's Malpighian tubules so slowly that whefl,
after a blood meal, the tubules rapidly eliminate a volume of fluid equivalent to 5-10
times that of the haemolymph, there is a loss of only about 2 % of the haemolymph
content of amino acids (Maddrell & Gardiner, 1980). No reabsorption of amino acids
is required during this rapid excretion of fluid.
Insect Malpighian tubules thus have only limited permeability to haemolymph
solutes. Three questions now arise, (i) How can such low permeability be reconciled
with the overriding need, emphasized above, for an excretory system to contain a
relatively non-selective and permeable nitration site ? (ii) How are the walls of
Malpighian tubules structurally organized to provide a low effective permeability ?
(iii) What are the advantages to be derived from having an excretory system of only
limited permeability to haemolymph solutes ?
It will be the main object of the remainder of this paper to answer these questions.
OPERATION OF AN EXCRETORY SYSTEM OF LOW PERMEABILITY
To answer the first question, it has to be pointed out that although such small
solutes as amino acids can only penetrate the walls of insect Malpighian tubules
slowly, the tubules yet have measurable permeabilities to substances as large as inulin
(Ramsay & Riegel, 1961; Maddrell & Gardiner, 1974). This is a clear indication that
the apparently low overall permeability of the tubule wall might be due more to a
limitation in area of the permeable sites than to any restriction at the sites of permeation.
This is very important, as it means that toxic molecules, even those of moderate
size, will still be removed passively, albeit slowly, from the insect's haemolymph.
This in turn suggests that insects might in fact use the same basis for the operation
of their excretory systems as do other animals, but that the rate of 'filtration' of the
extracellular fluid is very much reduced. But how are insects able to survive with
such a slowly operating system and gain the advantages described below, when other
animals seem not to be able to ?
A possible explanation is along the following lines. Insects as a group are
characterized by their small bodily size, which gives them a high surface-area/volume
ratio and makes their body fluids more liable to be affected by changes in the environment.
In spite of this, insects seem only to be found in habitats which impose some
form of osmotic and/or ionic stress (thus they appear on land, and in fresh, brackish,
and hypersaline bodies of water, but not in such a stable environment as the sea). Of
course, a crucial element in their ability to survive in such environments is the
possession of a wax-covered integument which greatly restricts ion and water fluxes
between their internal and external environments (Beament, 1961). It is often thought
that the haemolymph of insects, because of its supposedly large volume, might also
help in that it could act as a water store and as a buffer against changes in composition.
While this could be true for some insects, such as caterpillars, which have particularly
large volumes of haemolymph, recent measurements of haemolymph volume in other
insects make this less likely. They show that many insects, particularly flying insects,
have haemolymph volumes which are, if anything, smaller in relation to total body
weight than, for example, the extracellular fluid of vertebrates. Table 1 shows the
results of determinations of haemolymph volume in a series of insects. These resul
are to be compared with determinations of extracellular fluid volume in vertebrate^.